Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2

Forest ecosystems are important sinks for rising concentrations of atmospheric CO2. In previous research, we showed that net primary production (NPP) increased by 23 ± 2% when four experimental forests were grown under atmospheric concentrations of CO2 predicted for the latter half of this century. Because nitrogen (N) availability commonly limits forest productivity, some combination of increased N uptake from the soil and more efficient use of the N already assimilated by trees is necessary to sustain the high rates of forest NPP under free-air CO2 enrichment (FACE). In this study, experimental evidence demonstrates that the uptake of N increased under elevated CO2 at the Rhinelander, Duke, and Oak Ridge National Laboratory FACE sites, yet fertilization studies at the Duke and Oak Ridge National Laboratory FACE sites showed that tree growth and forest NPP were strongly limited by N availability. By contrast, nitrogen-use efficiency increased under elevated CO2 at the POP-EUROFACE site, where fertilization studies showed that N was not limiting to tree growth. Some combination of increasing fine root production, increased rates of soil organic matter decomposition, and increased allocation of carbon (C) to mycorrhizal fungi is likely to account for greater N uptake under elevated CO2. Regardless of the specific mechanism, this analysis shows that the larger quantities of C entering the below-ground system under elevated CO2 result in greater N uptake, even in N-limited ecosystems. Biogeochemical models must be reformulated to allow C transfers below ground that result in additional N uptake under elevated CO2.

[1]  John McGregor,et al.  Ecosystems , 2009, J. Object Technol..

[2]  H. Owen,et al.  New Phytol , 2008 .

[3]  R. Ceulemans,et al.  Increased nitrogen-use efficiency of a short-rotation poplar plantation in elevated CO(2) concentration. , 2007, Tree physiology.

[4]  Richard P Phillips Towards a rhizo-centric view of plant-microbial feedbacks under elevated atmospheric CO2. , 2007, The New phytologist.

[5]  M. G. Ryan,et al.  Aboveground sink strength in forests controls the allocation of carbon below ground and its [CO2]-induced enhancement , 2006, Proceedings of the National Academy of Sciences.

[6]  Karl Rohr,et al.  Limits on Estimating the Width of Thin Tubular Structures in 3D Images , 2006, MICCAI.

[7]  W. Morris,et al.  CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. , 2006, Ecology.

[8]  R. Ceulemans,et al.  Woody biomass production during the second rotation of a bio‐energy Populus plantation increases in a future high CO2 world , 2006 .

[9]  J. Hobbie,et al.  15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. , 2006, Ecology.

[10]  Jarrett J. Barber,et al.  Long-term Effects of Free Air CO2 Enrichment (FACE) on Soil Respiration , 2006 .

[11]  R. Norby,et al.  Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. , 2006, Ecology.

[12]  R. B. Jackson,et al.  Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. , 2006, Ecology.

[13]  M. Hoosbeek,et al.  Free Atmospheric CO2 Enrichment (FACE) Increased Labile and Total Carbon in the Mineral Soil of a Short Rotation Poplar Plantation , 2006, Plant and Soil.

[14]  Haegeun Chung,et al.  Fungal community composition and metabolism under elevated CO2 and O3 , 2006, Oecologia.

[15]  R. Ceulemans,et al.  Forest response to elevated CO2 is conserved across a broad range of productivity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[16]  E. P. McDonald,et al.  Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2 , 2005 .

[17]  Carlo Calfapietra,et al.  Canopy profiles of photosynthetic parameters under elevated CO2 and N fertilization in a poplar plantation. , 2005, Environmental pollution.

[18]  M. Gonzalez-Meler,et al.  Accelerated belowground C cycling in a managed agriforest ecosystem exposed to elevated carbon dioxide concentrations , 2005 .

[19]  K. Pregitzer,et al.  Scaling ozone responses of forest trees to the ecosystem level in a changing climate , 2005 .

[20]  A. Polle,et al.  Leaf litter production and decomposition in a poplar short‐rotation coppice exposed to free air CO2 enrichment (POPFACE) , 2005 .

[21]  H. Rouhier,et al.  Effect of elevated CO2 on carbon and nitrogen distribution within a tree (Castanea sativa Mill.) — soil system , 1994, Plant and Soil.

[22]  K. Treseder A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. , 2004, The New phytologist.

[23]  D. Ellsworth,et al.  Canopy position affects photosynthetic adjustments to long-term elevated CO2 concentration (FACE) in aging needles in a mature Pinus taeda forest. , 2004, Tree physiology.

[24]  W. Parton,et al.  Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide , 2004 .

[25]  R. Norby,et al.  Effects of elevated CO2 on nutrient cycling in a sweetgum plantation , 2004 .

[26]  N. E. Miller,et al.  Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Norby,et al.  A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments , 2004 .

[28]  R. Norby,et al.  Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand , 2004 .

[29]  M. Lukac,et al.  More new carbon in the mineral soil of a poplar plantation under Free Air Carbon Enrichment (POPFACE): Cause of increased priming effect? , 2004 .

[30]  Dale W. Johnson,et al.  Elevated CO2, rhizosphere processes, and soil organic matter decomposition , 1998, Plant and Soil.

[31]  E. Zagal Influence of light intensity on the distribution of carbon and consequent effects on mineralization of soil nitrogen in a barley (Hordeum vulgare L.)-soil system , 1994, Plant and Soil.

[32]  C. Field,et al.  Allocating leaf nitrogen for the maximization of carbon gain: Leaf age as a control on the allocation program , 1983, Oecologia.

[33]  N. E. Nielsen,et al.  Effect of extracellular-enzyme activities on solubilization rate of soil organic nitrogen , 2004, Biology and Fertility of Soils.

[34]  Monica G. Turner,et al.  Ecological Thresholds: The Key to Successful Environmental Management or an Important Concept with No Practical Application? , 2006, Ecosystems.

[35]  K. Pregitzer,et al.  Soil nitrogen transformations under Populus tremuloides, Betula papyrifera and Acer saccharum following 3 years exposure to elevated CO2 and O3 , 2003 .

[36]  R. Norby,et al.  Soil microbial activity in a Liquidambar plantation unresponsive to CO2-driven increases in primary production , 2003 .

[37]  R. Ceulemans,et al.  Free-air CO2 enrichment (FACE) enhances biomass production in a short-rotation poplar plantation. , 2003, Tree physiology.

[38]  R. Norby,et al.  Leaf dynamics of a deciduous forest canopy: no response to elevated CO2 , 2003, Oecologia.

[39]  Pete Smith,et al.  Europe's Terrestrial Biosphere Absorbs 7 to 12% of European Anthropogenic CO2 Emissions , 2003, Science.

[40]  M. Lukac,et al.  Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE). , 2003 .

[41]  W. Schlesinger,et al.  Soil–Nitrogen Cycling in a Pine Forest Exposed to 5 Years of Elevated Carbon Dioxide , 2003, Ecosystems.

[42]  J. Pérez‐Moreno,et al.  Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? , 2003, The New phytologist.

[43]  W. Schlesinger,et al.  The nitrogen budget of a pine forest under free air CO2 enrichment , 2002, Oecologia.

[44]  W. Schlesinger,et al.  Forest carbon balance under elevated CO2 , 2002, Oecologia.

[45]  R. Phillips,et al.  Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone , 2002, Oecologia.

[46]  J. Houghton,et al.  Climate change 2001 : the scientific basis , 2001 .

[47]  J. Isebrands,et al.  Photosynthesis, light and nitrogen relationships in a young deciduous forest canopy under open‐air CO2 enrichment , 2001 .

[48]  W. Schlesinger,et al.  The influence of elevated atmospheric CO2 on fine root dynamics in an intact temperate forest , 2001 .

[49]  A. Hodge,et al.  An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material , 2001, Nature.

[50]  P. Ciais,et al.  Consistent Land- and Atmosphere-Based U.S. Carbon Sink Estimates , 2001, Science.

[51]  G. Katul,et al.  Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere , 2001, Nature.

[52]  F. Miglietta,et al.  Free‐air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system , 2001 .

[53]  R. Norby,et al.  Allometric determination of tree growth in a CO2‐enriched sweetgum stand , 2001 .

[54]  W. Schlesinger,et al.  Soil CO2 dynamics, acidification, and chemical weathering in a temperate forest with experimental CO2 enrichment , 2001 .

[55]  D. Ellsworth,et al.  Forest litter production, chemistry and decomposition following two years of Free-Air CO2 Enrichment , 2001 .

[56]  W. Schlesinger,et al.  Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem , 2000 .

[57]  Jürgen K. Friedel,et al.  Review of mechanisms and quantification of priming effects. , 2000 .

[58]  William H. McDowell,et al.  Long-Term Nitrogen Additions and Nitrogen Saturation in Two Temperate Forests , 2000, Ecosystems.

[59]  P. Curtis,et al.  INTERACTIVE EFFECTS OF ATMOSPHERIC CO2 AND SOIL‐N AVAILABILITY ON FINE ROOTS OF POPULUS TREMULOIDES , 2000 .

[60]  P. Curtis,et al.  Atmospheric Co2, Soil‐N Availability, And Allocation Of Biomass And Nitrogen By Populus Tremuloides , 2000 .

[61]  R. E. Dickson,et al.  Effects of Tropospheric O3 on Trembling Aspen and Interaction with Co2: Results from an O3-Gradient and a Face Experiment , 1999 .

[62]  James F. Reynolds,et al.  VALIDITY OF EXTRAPOLATING FIELD CO2 EXPERIMENTS TO PREDICT CARBON SEQUESTRATION IN NATURAL ECOSYSTEMS , 1999 .

[63]  C. Field,et al.  Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands , 1999, Oecologia.

[64]  J. Nagy,et al.  A free‐air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2 , 1999 .

[65]  S. Bridgham,et al.  Nutrient efficiency along nutrient availability gradients , 1999, Oecologia.

[66]  R. Ceulemans,et al.  Elevated atmospheric CO2 increases fine root production, respiration, rhizosphere respiration and soil CO2 efflux in Scots pine seedlings , 1998 .

[67]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[68]  M. Chalot,et al.  Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. , 1998, FEMS microbiology reviews.

[69]  Steven W. Leavit Biogeochemistry, An Analysis of Global Change , 1998 .

[70]  Vemap Participants Vegetation/ecosystem modeling and analysis project: Comparing biogeography and biogeochemistry models in a continental-scale study of terrestrial ecosystem responses to climate change and CO2 doubling , 1995 .

[71]  J. Amthor Terrestrial higher‐plant response to increasing atmospheric [CO2] in relation to the global carbon cycle , 1995 .

[72]  R. McMurtrie,et al.  Long-Term Response of Nutrient-Limited Forests to CO"2 Enrichment; Equilibrium Behavior of Plant-Soil Models. , 1993, Ecological applications : a publication of the Ecological Society of America.

[73]  A. Mannion The earth as transformed by human action , 1991 .

[74]  Robert W. Howarth,et al.  Nitrogen limitation on land and in the sea: How can it occur? , 1991 .

[75]  J. A. Veen,et al.  15N-Nitrogen mineralization from bacteria by protozoan grazing at different soil moisture regimes , 1991 .

[76]  D. Read,et al.  Proteinase activity in mycorrhizal fungi. II. The effects of mineral and organic nitrogen sources on induction of extracellular proteinase in Hymenoscyphus ericae (Read) Korf & Kernan. , 1990 .

[77]  J. Aber,et al.  Nitrogen saturation in northern forest ecosystems , 1989 .

[78]  C. Sabine,et al.  Global Carbon Cycle , 2014 .

[79]  B. Turner The Earth as Transformed by Human Action , 1988 .

[80]  R. Aerts,et al.  Nitrogen-use efficiency : a biologically meaningful definition? , 1987 .

[81]  D. Read,et al.  The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. III: Protein utilization by Betula, Picea and Pinus in mycorrhizal association with Hebeloma crustuliniforme , 1986 .

[82]  M. Clarholm Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen , 1985 .

[83]  Peter M. Vitousek,et al.  Nutrient Cycling and Nutrient Use Efficiency , 1982, The American Naturalist.

[84]  Stephan Kempe,et al.  The Global Carbon Cycle. , 1979 .

[85]  S. Goldhor Ecology , 1964, The Yale Journal of Biology and Medicine.

[86]  H. Cowles Forestry , 1907, Botanical Gazette.